BRAZILIAN JOURNAL OF OCEANOGRAPHY, 62(2):89-102, 2014

TROPHIC GROUPS OF DEMERSAL FISH OF SANTOS BAY AND ADJACENT CONTINENTAL SHELF, SÃO PAULO STATE, BRAZIL: TEMPORAL AND SPATIAL COMPARISONS

Elizabeti Y. Muto1,*, Thaïs Navajas Corbisier1, Leandro Inoe Coelho1, Lidia Paes Leme Arantes1, André Chalom2 and Lucy Satiko Hashimoto Soares1

1Instituto Oceanográfico da Universidade de São Paulo (Praça do Oceanográfico, 191, 05508-120 São Paulo, SP, Brasil)

2Instituto de Matemática e Estatística da Universidade de São Paulo (Rua do Matão 1010, 05508-050 São Paulo, SP, Brasil)

*Corresponding author: [email protected] http://dx.doi.org/10.1590/S1679-87592014045906202

A B S T R A C T

The temporal and spatial variations of feeding habits and trophic groups of demersal fish species of Santos Bay and the adjacent continental shelf were investigated. The samples were taken in September 2005 and March 2006 by bottom otter trawling. The stomach content analysis of 2,328 specimens of 49 species showed most fish fed on a large range of food items but relied heavily on shrimp, crabs/swimming-crabs, amphipods, mysids, polychaetes, ophiuroids, squids, and teleosteans. The species were classified into ten trophic groups. Shrimp were an important food source in the Santos bay and inner shelf, while ophiuroids were important prey for predators of the middle shelf. Many species relied on crabs/swimming-crabs during the summer, especially on the middle shelf. The spatial and temporal variability in food resource utilization by fish were related to the pattern of distribution and abundance of their prey. The predation on shrimp and crabs/swimming-crabs seems to be related to the water mass dynamics of the region. Intraspecific comparisons demonstrated that most of the species display spatial and/or temporal variation in their diet. The demersal ichtyofauna can also be divided into the more general categories of piscivores, nektonic invertebrate feeders, benthic invertebrate feeders and planktonic invertebrate feeders.

R E S U M O

A variação temporal e espacial dos hábitos alimentares e dos grupos tróficos de peixes demersais abundantes na baía de Santos e plataforma continental adjacente foi investigada. As amostras foram obtidas em setembro de 2005 e março de 2006, utilizando-se rede de arrasto de fundo. A análise dos conteúdos estomacais de 2.328 exemplares de 49 espécies demonstrou que a maioria se alimentou de uma grande variedade de presas, destacando-se os camarões, caranguejos/siris, anfípodes, misidáceos, poliquetas, ofiuróides, lulas e teleósteos. De acordo com as presas principais, os peixes foram agrupados em dez grupos tróficos. Os camarões foram presas importantes na baía e plataforma interna, e os ofiuróides apenas na plataforma média. Caranguejos/siris tiveram grande importância na dieta de várias espécies durante o verão, em especial na plataforma média. A variação espacial e temporal na alimentação dos peixes esteve associada ao padrão de distribuição e abundância de suas presas. A ingestão de camarões e caranguejos/siris está, provavelmente, associada à dinâmica das massas de água na região. Comparações intraespecíficas demonstraram que a maioria das espécies apresenta variação espacial e/ou temporal na dieta. A ictiofauna demersal pode ser categorizada em grupos tróficos mais abrangentes: piscívoros, comedores de invertebrados nectônicos, comedores de invertebrados bentônicos e comedores de invertebrados planctônicos.

Descriptors: Diet, Stomach content, Marine fish, Teleostei, Elasmobranchii, Southeastern Brazil. Descritores: Dieta, Conteúdos estomacais, Peixes marinhos, Teleostei, Elasmobranchii, Sudeste do Brasil.

INTRODUCTION (419,400 inhab.) and São Vicente (332,445 inhab.) being the most heavily populated (IBGE, 2010). It The Baixada Santista is the main tourist constitutes a complex ecosystem with brackish and coastal area of São Paulo State; its metropolitan region marine waters, islands, internal channels, estuaries, encompasses nine municipalities, with Santos mangrove forests, and rainforest. Monitored by the

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State Environmental Agency (CETESB) since 1980, mentioning (SOARES et al., 1992; SOARES et al., part of its marine zone was officially proclaimed as a 1993; PIRES-VANIN et al., 1993; SOARES et al., Conservation Unit of Sustainable Use (SÃO PAULO, 2008). 2008a). It is an area subject to great environmental The present study was carried out in support impacts, with many sources of anthropogenic of the project ECOSAN-subproject Trophodynamics, pollution. The sewage disposal from the Santos and which assessed the food web of the Santos region São Vicente estuaries promotes the eutrophication of using stable isotopes (SI) of carbon (δ13C) and Santos Bay and neighboring coastal waters, mainly nitrogen (δ15N). While stable isotopes (SI) indicate the during the summer. In addition to the port of Santos main sources of energy for consumers based on the (the most important in Brazil), the industrial complex assimilated food (PETERSON; FRY, 1987), stomach of Cubatão is responsible for the great volume of content data provide the taxonomic status of the prey industrial effluents in the coastal region. ingested, and together with natural history information Marine and estuarine fisheries are an provide additional insights to support SI conclusions important economic activity; the landings in Santos (PETERSON, 1999). We selected dominant species in were responsible for ~60% of the total catch of São the region as well as those representing important food Paulo State in 2010 (22,094.6 t) and 2011 (20,931.9 t) habits. The species surveyed made up 92% and 85% (INSTITUTO DE PESCA, 2011, 2012). The sciaenids of the abundance in Santos Bay (DIAS, J.F., pers. are the main target of the regional fishery, especially comm.) and continental shelf (DIAS et al., 2008), the white mouth, Micropogonias furnieri; the Jamaica respectively. Of the 49 species analyzed, 8.2% are weakfish, Cynoscion jamaicensis; and the king threatened with extinction (Atlantoraja cyclophora, weakfish, Macrodon atricauda (VALENTINNI et al., Urophycis brasiliensis, Cynoscion jamaicensis, and 1991; ÁVILA-DA-SILVA et al., 2005). Paralichthys patagonicus) and 14.3% (Lophius Information on the diversity and temporal gastrophysus, Merluccius hubbsi, Macrodon and spatial variation of the demersal ichthyofauna are atricauda, Micropogonias furnieri, Umbrina canosai, available for the continental shelf located to the north and two elasmobranchs - Rioraja agassizii and of the area studied (ROSSI-WONGTSCHOWSKI; Rhinobatos percelens) are overexploited in São Paulo PAES, 1993; ROCHA; ROSSI-WONGTSCHOWSKI, State (SÃO PAULO, 2008b). Therefore, 1998; MUTO et al., 2000). However, there are fewer understanding the biology of these species and their data for the present study site. The estuarine complex role in the ecosystem is critical for monitoring of Santos-São Vicente represents one of the most programs. Specifically, this study sought to identify important nursery grounds for the ichthyofauna, the diet of dominant fish species of Santos Bay and the characterized by high fish diversity and abundance continental shelf and the trophic structure of the fish (PAIVA FILHO et al., 1987). The sciaenid fish are the assemblage. The temporal and spatial variability of the most abundant family in Santos Bay all year round trophic groups were also assessed. (GIANNINI; PAIVA FILHO, 1990). Human activities influence fish diversity and promote changes in the MATERIAL AND METHODS trophic interactions. For example, the replacement of long-lived piscivore fish by small planktivore fish and Sampling invertebrates in the overall fishery landings indicates the impact of fishing on the structure of marine food The samples were collected during two webs, affecting the abundance of top predators and research cruises conducted from 9 to 15 September promoting long-term changes in the number of species (late austral winter, W) and 1 to 6 March 2006 (late (PAULY et al., 1998; PAULY; WATSON, 2005). austral summer, S) on board the Research Vessel Prof. Identification of food web linkages is a W. Besnard (Oceanographic Institute, University of major goal in ecology because it provides basic São Paulo) within the scope of the project “The information on trophic flows and the potential for Influence of the estuarine complex of the Baixada interspecific interactions (REUM; ESSINGTON, Santista on the adjacent continental shelf''s ecosystem 2008). Dietary data are essential to trace these (ECOSAN) - subproject Trophodynamics”. Fish were linkages, enabling managers to cope with complex collected using a bottom otter trawl with a 17-m net issues, such as biological control, conservation, and (60-mm stretch-mesh in the body and sleeve and 25 fishery management. Many studies have been mm at the cod end), and frozen at -20ºC. Fifteen and conducted to clarify the trophic relationships of the thirty-minute hauls at the speed of 2 knots were coastal fish of Southeastern Brazil; however, the carried out in Santos Bay and on the continental shelf, comprehensive studies carried out for the demersal respectively. The fishing was conducted in two fish assemblage off Ubatuba and São Sebastião shelf areas of Santos Bay (A1, A2; depth = 8.9 to 11 m) (north coast of São Paulo) showing the main energy and six areas on the continental shelf, four of them pathway supporting fish production are worth located on the inner shelf (IS: A3, A4, A7, P9; depth =

MUTO ET AL.: TROPHIC GROUPS OF DEMERSAL FISH 91

19.8 to 26.5 m) and two on the middle shelf (MS: A5, percentage of mass of preyi in relation to the total A6; depth = 56 to 57 m) (Fig. 1). During the winter, mass of all prey in the sample) of each prey category the A5 area was not sampled due to poor weather for each species were calculated in accordance with conditions. All diet analyses were performed Hyslop (1980). Empty stomachs, as well as those with combining areas with similar depths; thus from now food remains difficult to identify at any taxonomic on these depth-areas will be referred to as regions. The level, were excluded from the analysis. The trawling operation was repeated in some sites importance of each prey category was evaluated whenever fish samples were scarce for diet through the Feeding Index (FI%) of Kawakami; analyses. In the laboratory, each specimen was Vazzoler (1980), using mass instead of volume: measured (total length, mm) and weighed (to the nearest 0.1 g). For the elasmobranchs, the disc length FIi % = Fi % × Mi % /  Fi % × Mi % × 100 was measured (from the tip of the snout to the posterior lobe of the pectoral fin). The stomachs were The FI% was calculated for each species, by removed, preserved in formalin (10%), and transferred sampling region (Santos Bay, inner shelf, and middle to alcohol (70%) for gut analysis. shelf) and period (March and September). The prey items were identified under The multivariate analysis was carried out on stereomicroscope at different taxonomic levels, the total FI % matrix, using the statistical package depending on the preservation of their bodies. Caridea PRIMER 6 (CLARKE; WARWICK, 2001). Nine and Dendrobranchiata decapods were referred to as samples of each of nine species were excluded from shrimp, while Brachyura and Anomura were classified this analysis. Prey categories with FI smaller than 5% as crabs. For each prey category, we registered the were pooled in the “other prey” category. Diet overlap occurrence (presence) and mass (0.001g). among species (sample size > 5) was evaluated Data analysis through cluster analyses (Q-mode), using the Bray- Curtis similarity index and the Group Average The prey were grouped into defined method. The trophic groups were arbitrarily categories and weighed (0.001g) according to season established at the limit of 50% of diet similarity; and and region of sampling. The frequency of occurrence to detect the average prey contribution to each group (F %, the number of stomachs containing a specific i the SIMPER routine in PRIMER 6 was used. preyi expressed as a percentage of all stomachs examined for the species) and relative mass (Mi %,

Fig. 1. Map showing the areas sampled in Santos Bay (upper frame) and adjacent continental shelf

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RESULTS (Pellona harroweri) to 45.7 cm (Zapteryx brevirostris) in winter 2005 (Fig. 2). Excluding Trichiurus lepturus A total of 2,328 individuals of 49 species (107 cm) and Paralichthys patagonicus (56 cm) (Table 1) were investigated for diet composition because of their small sample sizes (n=1), in summer analysis, most of them collected in summer 2006 (70.5 2006 the mean size ranged from 8.9 cm (Anchoa %). The mean size of the species ranged from 5.6 cm filifera) to 53.4 cm (Z. brevirostris) (Fig. 3).

Table 1. Taxonomic list of fish species analyzed and respective codes. B = bay, IS = inner shelf, MS = middle shelf.

Order Family Species Codes Rajiformes Rajidae Atlantoraja cyclophora ATCY Psammobatis extenta PSEX Rhinobatidae Rhinobatos percellens RHPE Zapteryx brevirostris ZABR Clupeiformes Engraulidae Anchoa filifera ANFI Pristigasteridae Chirocentrodon bleekerianus CHBL Pellona harroweri PEHA Clupeidae Harengula clupeola HACL Siluriformes Ariidae Cathorops spixii CASP Ophidiiformes Ophidiidae Raneya brasiliensis RABR Gadiformes Phycidae Urophycis brasiliensis URBR Merlucciidae Merluccius hubbsi MEHU Batrachoidiformes Batrachoididae Porichthys porosissimus POPO Lophiiformes Lophiidae Lophius gastrophysus LOGA Scorpaeniformes Dactylopteridae Dactylopterus volitans DAVO Triglidae Prionotus punctatus PRPU Prionotus nudigula PRNU Serranidae Serranus auriga SEAU Carangidae Chloroscombrus chrysurus CHCH nobilis CONO Selene setapinnis SESE Trachurus lathami TRLA Gerreidae Diapterus rhombeus DIRH Eucinostomus argenteus EUAR Orthopristis ruber ORRU Sciaenidae Ctenosciaena gracilicirrhus CTGR Cynoscion jamaicensis CYJA Larimus breviceps LABR Isopisthus parvipinnis ISPA Nebris microps NEMI Macrodon atricauda MAAN Menticirrhus americanus MEAM Micropogonias furnieri MIFU Paralonchurus brasiliensis PABR Stellifer brasiliensis STBR Stellifer rastrifer STRA Umbrina canosai UMCA Mullidae Mullus argentinae MUAR Upeneus parvus UPPA Percophidae Percophis brasiliensis PEBR Pleuronectiformes Trichiuridae Trichiurus lepturus TRLE Paralichthyidae Etropus crossotus ETCR Etropus longimanus ETLO Paralichthys isocelles PAIS Paralichthys patagonicus PAPAT Paralichthys triocellatus PATR Xystreurys rasile XYRA Tetraodontiformes Monacanthidae Stephanolepis hispidus STHI Tetraodontidae Lagocephalus laevigatus LALA

MUTO ET AL.: TROPHIC GROUPS OF DEMERSAL FISH 93

Fig. 2. Mean length (± standard deviation) of fish species analyzed in Santos Bay (white diamond), inner shelf (gray diamond), and middle shelf (black diamond) during the winter 2005. * disc length

Fig. 3. Feeding index (%) of prey items of fish species sampled in Santos Bay, inner shelf, and middle shelf during the winter 2005. Size of the sample is indicated in brackets. See table 1 for species codes.

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Fig. 4. Feeding index (%) of prey items of fish species sampled in Santos Bay, inner shelf and middle shelf during the winter 2005. Size of the sample is indicated in brackets. See table 1 for species codes

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Fig. 5. Feeding index (%) of prey items of fish species sampled in Santos Bay, inner shelf and middle shelf during the summer 2006. Size of the sample is indicated in brackets. See table 1 for species codes

Diet Ophiuroidea, Crustacea unidentified (un.), Copepoda, Peracarida un., , Cumacea, Isopoda, The taxonomic list of the prey identified in , Decapoda un., shrimp, crabs, Cephalopoda the stomach contents and the frequency of occurrence un., Bivalvia, squids, and Teleostei. The remaining and relative mass of the main prey groups are prey categories were grouped into “other items”. presented (Appendix). Because of their importance in On the whole, during the winter the diet the diet, the following prey categories were used in the compositions of the fish species in Santos Bay (B) cluster analysis and figures: Hydrozoa, Polychaeta, were closely similar to those of the inner shelf (IS)

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(Fig. 4). Teleosteans, shrimp, polychaetes, and mysids (amphipod and polychaete feeders) during the were the predominant prey in both areas. Crabs, summer. amphipods, hydrozoans and bivalves contribute greatly to the diet of some species of the bay, while Specific Spatio-Temporal Comparisons copepods made up a small part of the diet of two species. Squids were the main food for one species of Spatial comparisons performed for winter the IS. Although ostracods represented 92% (FI) of the samples showed that Isopisthus parvipinnis, Larimus diet of Harengula clupeola, the sample size was too breviceps and Paralonchurus brasiliensis of the bay small to characterize the diet of the species. On the and IS stayed in the same trophic group (TG), while middle shelf (MS), ophiuroids were prominent in the Pellona harroweri moved from the piscivore group diet of many species, in addition to shrimp, crabs, and (G7) in the bay to shrimp and crustacean unidentified polychaetes. Isopods were important food for (un.) feeder group (G3) on the IS. In the summer, most Porichthys porosissimus, while bivalves made a minor of the species (87.5%) occurring in at least two areas contribution to the diet of Dactylopterus volitans. displayed contrasting diets; with the exception of During summer 2006, the diet composition Paralonchurus brasiliensis that fed on polychaetes in of the fish assemblage was more diversified. both bay and IS (Table 3). Teleosteans, polychaetes, and shrimp were important Specific seasonal dietary differences in the prey in Santos Bay and IS; crabs and copepods were bay occurred for four species (50%), while three especially important for some species in the IS (Fig. piscivores (I. parvipinnis, P. harroweri and Trichiurus 5). For some species of the bay (Menticirrhus lepturus) and one polychaete feeder (Micropogonias americanus, Prionotus punctatus, and Pellona furnieri) stayed in the same TG. Among the five harroweri), amphipods were also important food species of the IS and four of the MS, only items. In the MS, Teleosteans and crabs were the most Menticirrhus americanus (IS) and Raneya brasiliensis exploited prey. Ophiuroids, squids, polychaetes, (MS) exploited the same prey type in both periods amphipods, isopods, and shrimp contributed greatly to (Table 3). the diets of some species. Cumaceans and copepods were of minor importance for the species of the middle DISCUSSION shelf.

Trophic Groups (TG) The fish assemblage of the Santos region used a broad range of food sources, comprising The cluster analysis showed 10 major nektonic, planktonic, and benthic organisms of the trophic groups for the 46 fish species examined (Table infauna, epifauna, and suprabenthos. The most 3, Fig. 6): G1 = teuthophagous (squids); G2 = representative prey were decapods (shrimp and crabs), crustacean unidentified (un.) and shrimp feeders; G3 amphipods, mysids, copepods, squids, polychaetes, = shrimp and crustacean (un.) feeders; G4 = shrimp, ophiuorids, and bony fish. The coastal demersal fish of polychaete, and crustacean (un.) feeders; G5 = Santos feed on similar food resources to those mysid and crustacean (un.) feeders; G6 = crab and exploited by the fish community of the soft bottom crustacean (un.) feeders; G7 = piscivores (teleosteans); shelf worldwide. For example, in the tropical bay of G8 = ophiuroid and crab feeders; G9 = polychaete Thailand (depth < 5 m), the fish community (28 feeders; G10 = amphipod and polychaete feeders. The species) feed on a variety of prey, especially on G2 and G3 groups differed in their contribution of calanoid copepods and shrimp; however, the feeding shrimp and crustacean unidentified to the diet. The variability is influenced by monsoon-seasons and prey contributions (%) to the species grouping within substrate type (sandy or muddy bottom) a specific TG are represented in Table 2. Four sample (HAJISAMAE; IBRAHIM, 2008). In addition to species were not included in any group: Cathorops copepods and shrimp, fish and gammaridean spixii (Bwinter) feeding on hydrozoans, Harengula amphipods are also included among the main food clupeola (ISsummer) on copepods, Lagocephalus items of 48 bottom fish species sampled in the coastal laevigatus (ISsummer) on decapods unidentified, and areas (mean depths = 12.3 to 19.8 m) of Thailand Porichthys porosissimus (MSsummer) on crustacean (HAJISAMAE, 2009). On the continental shelf off unidentified, shrimp, and isopods (Fig. 6). Mexico, decapods are the main prey for most demersal Shrimp (G3), teleostean (G7), and fish from depths of 20 to 80 m, in addition to polychaete (G9) feeder groups included most of the mollusks, and fish (PÉREZ-ESPAÑA et al., 2005). fish species, with 12, 10, and 10, respectively (Table Off the west coastal of Australia (depth = 5-35 m), 3, Figure 6). The G8 group (ophiuroid and crab polychaetes, crustaceans, mollusks, echinoderms, and feeders) was exclusive to the MS. The G5 (mysid fish represent the major prey for 18 benthic fish feeders) occurred only during the winter, the G10 (PLATELL; POTTER, 2001). Most of the benthic fish

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(102 species) off the Southeastern Australia shelf feed addition to fish, cephalopods, and pelagic on benthic prey; pelagic invertebrates and fish are invertebrates (SEDBERRY et al., 1979). A large scale important for some species (BULMAN et al., 2001). study based on a comprehensive literature review Off the continental shelf of Colombia, the main food covering 60 fish species of the Southeastern shelf of types for 30 species are benthic crustaceans (crabs, the United States showed three dominant trophic shrimp, and stomatopods) and bony fish (LÓPEZ- guilds: piscivores, carnivores and browsers PERALTA; ARCILA, 2002). Macrobenthic (MARANCIK; HARE, 2007). The carnivores feed invertebrates (amphipods, decapods, and polychaetes) mainly on fish and invertebrates, while browsers on are the main food items for nine dominant fish of the bryozoans, algae, poriferans, hydrozoans, and outer shelf of New Jersey and Delaware (US), in anthozoans.

Fig. 6. Dendrogram showing the trophic groups of fish sampled in Santos Bay (circle), inner shelf (triangle) and middle shelf (inverted triangle) during the winter (W = September 2005, closed symbols) and summer (S = March 2006, open symbols).

Trophic groups: G1 = teuthophagous; G2 = crustacean unidentified (un.) and shrimp feeders; G3 = shrimp and crustacean (un.) feeders; G4 = shrimp, polychaete, and crustacean (un.) feeders; G5 = mysid and crustacean (un.) feeders; G6 = crab and crustacean (un.) feeders; G7 = piscivores; G8 = ophiuroid and crab feeders; G9 = polychaete feeders; G10 = amphipod and polychaete feeders. See table 1 for fish species codes

Table 2. Results of the SIMPER analysis showing the average prey contribution (cumulative 90 %) to each trophic group of the dendrogram. un. = unidentified

MAIN PREY TROPHIC GROUPS Squids Crustacean un. Shrimp Crabs Mysida Amphipoda Polychaeta Ophiuroidea Teleostei G1 95.2 G2 87.8 7.4 G3 8.3 87.0 G4 5.3 51.3 33.8 G5 15.0 84.5 G6 5.2 86.8 G7 91.8 G8 7.1 88.7 G9 95.1 G10 69.8 29.3

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Table 3. Summary of species composition, main prey, and number of species (N) included in each trophic group. See table 1 for species codes. un. = unidentified

W I N T E R 2 0 0 5 S U M M E R 2 0 0 6

Trophic Main prey Bay Inner shelf Middle shelf Bay Inner shelf Middle shelf N groups

G1 Squid CONO PEBR, PAIS 3 G2 Crustacean un., CYJA POPO ANFI, CHBL, PEHA DAVO, TRLA 8 shrimp STBR G3 Shrimp, crustacean MAAT, MEAM, LABR MEAM, SESE, PSEX 12 un. NEMI, PEHA, UPPA, PRPU STRA ZABR G4 Shrimp, Polychaetes, PABR PABR DAVO, CTGR, 4 crustacean un. ZABR G5 Mysida, crustacean LABR LABR 1 un. G6 Crabs, crustacean un. STBR ATCY, PRPU, 5 PRNU, XYRA G7 Teleostei ISPA, ISPA ISPA, CHCH, CYJA LOGA, MEHU, 10 PEHA, PEHA, PATR, UPPA, TRLE TRLE URBR G8 Ophiuroidea, crabs CTGR, DAVO, MUAR, RABR, 7 RABR, STHI SEAU G9 Polychaetes MIFU ORRU CASP, DIRH, ETCR, CTGR, ZABR 10 MIFU, EUAR, PABR, PABR STHI G10 Amphipoda, MEAM ETLO 2 Polychaetes TOTAL 6 6 3 5 5 8

The diet composition of the species analyzed et al., 2008). Sergestids were the major shrimp in the in the Santos region was consistent with that found for diet of Selene setapinnis (G3), Macrodon atricauda the Southeastern region of Brazil (SOARES, 1989; (G3), and Nebris microps (G3) (pers. data), while SOARES et al., 1992; MUTO et al. 2001; SOARES; copepods were also important food items for VAZZOLER, 2001; CORRÊA et al., 2005; Chloroschombrus chrysurus (SIsummer), showing the CARVALHO; SOARES, 2006; VERA; SOARES, pelagic habits of those species. In contrast, most of the 2008; MARION et al., 2011; MUTO; SOARES, shrimp feeder fish of the continental shelf fed on the 2011), though the prey contributions to the diet are small carideans Leptochela and processids (pers. data). different for some species. The oblique mouth of Larimus breviceps suggests that On the northern continental shelf off São the mysids consumed by the species are of pelagic Paulo, the demersal fish community made up six habits, as found in Santos Bay and at Perequê Beach, trophic groups: pelagic piscivores; benthic piscivores; where L. breviceps feeds on sergestid shrimp and fish and/or pelagic prey feeders; fish and benthic mysids (RODRIGUES; MEIRA, 1988). Mysids are invertebrate (shrimp) feeders; benthic invertebrate more abundant on and just above the sea floor; feeders (brachyurans, shrimp, and amphipods); benthic however, in coastal waters, they perform a diel vertical invertebrate feeders (polychaetes, ophiuroids, and migration, ascending and dispersing into the water infaunal crustaceans) (SOARES et al., 2008). Similar column during the night (MURANO, 1999). The results were obtained in the present study. unidentified crustaceans consumed by Cynoscion The trophic groups found in the Santos jamaicensis during the winter might have been region can be further categorized as: a) piscivores, b) mysids, therefore this species belongs to the same nektonic invertebrate feeders, c) benthic invertebrate group as L. breviceps. feeders, and d) planktonic invertebrate feeders. The other species of the G2 group, Assuming that the unidentified crustaceans of the G2 Porichthys porosissimus (MSwinter), could be classified group are remains of those represented in the stomach as benthic invertebrate feeders, similar to those contents of each species, Chirocentrodon specimens from the MSsummer. The two individuals bleeckerianus (ISsummer), Pellona harroweri (ISsummer), from ISsummer fed on teleosteans; however, bigger Trachurus lathami (MSsummer), and Anchoa filifera specimens tend to rely on fish while the smaller ones (Bsummer), together with Harengula clupeola (ISsummer), on crustaceans (MUTO, 2004). Indeed, the mean size would compose the planktonic invertebrate feeders of P. porosissimus of the IS was 23.0 cm in contrast to group, since copepods and the pelagic shrimp 12.0 cm for specimens from the MS. Also, Stellifer sergestid and luciferid (OMORI, 1975) are the brasiliensis of G2 group is probably feeding on shrimp dominant food items for those species (pers. data, (G3), as found by Rodrigues; Meira (1988). Although unpublished; CARVALHO; SOARES, 2006; MUTO in summer Dactylopterus volitans fed on crabs and

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shrimp on the IS, the unidentified crustaceans MUTO et al., 2000; ROSSI-WONGTSCHOWSKI et consumed by this species on the MS might be crabs al., 2008) and invertebrates (PIRES-VANIN, 1993; because shrimp were not well represented in the diet PIRES-VANIN, 2008a) on the shelf. For instance, the of most species in the deeper area in this period, fish species Paralichthys patagonicus, Serranus suggesting the low availability of that prey. auriga, Merluccius hubbsi, Urophycis brasiliensis, Intraspecific spatial comparisons showed and Lophius gastrophysus, that usually occupy the that during the winter the species tended to feed on the outer domain of the shelf, follow the SACW same prey in the bay and IS; while in the summer, movement toward the shore during the summer most of the species underwent spatial dietary shifts, (ROSSI-WONGTSCHOWSKI; PAES, 1993). The feeding on shrimp on the IS and on different prey in abundance of the swimming crab Portunus the bay or MS. Temporal differences were prominent spinicarpus and the shrimp Xiphopenaeus kroyeri for most species, except for some sciaenids (Isopisthus alternates according to the water masses, the former is parvipinnis, Menticitthus americanus, Micropogonias related to the SACW frontal zone, and the later to the furnieri), Trichiurus lepturus, and Raneya brasiliensis. warm CW (PIRES, 1992). The seasonal pattern of The results highlight the complexity and plasticity of prey availability is reflected in the food resources used the trophic relationships of the demersal ichthyofauna by predators, modifying the trophic structure of the in the system, where variability occurred at species planktonic and demersal communities (PIRES- and community levels suggesting that different species VANIN et al., 1993). or population strata can have a particular trophic niche Changes in the species trophic guild may in a variable combination of time/space dimensions. depend not only on biological features but also on the The trophic plasticity allows fish species to cope with spatio-temporal changes in the ecological interactions the availability of their preferred prey in a variable between species (CARRASSÓN; CARTES, 2002). environment (GERKING, 1994). Within the scope of the project ECOSAN, the benthic The spatial and temporal variations of the megafauna of Santos Bay was sampled monthly trophic structure of the ichthyofauna of Santos can be during 2005, with higher abundances between January partially explained by the differential distribution of and July. In March and September the shrimp fish species as well as of their prey. The Xiphopenaeus kroyeri was the dominant species, oceanographic structure of the region was typical for followed by the swimming crabs Callinectes danae winter and summer seasons in the South Brazilian and C. ornatus (PIRES-VANIN et al., 2008b). Bight, with the interaction of three water masses: the Previous results in the study area showed that warm Coastal Water (CW; T > 20 ºC, S > 36.40), a polychaetes (W=winter=69%, S=summer=88%), mixture of continental freshwater and marine waters; mollusks (W=17%, S=5%), and crustaceans (W=12%, the oligotrophic Tropical Water (TW; temperature < S=3%) were the dominant benthic macrofauna 20 ºC, salinity > 36.40); and the nutrient enriched (HEITOR; TOMMASI, 2001). South Atlantic Central Water (SACW; T < 20 ºC, S < On the continental shelf, crustaceans were 36.40) (CASTRO FILHO; MIRANDA, 1998). the dominant megafaunal group in both seasons; Typically, the inner shelf is occupied by the CW and penaeid shrimp made up 66% of the total abundance the water column is vertically homogeneous due to a during the winter 2005, followed by brachyurans mixing process induced by wind stress and tidal shear. (16%) and asteroids (9%). In the summer 2006, The waters on the inner and middle shelf are separated brachyurans (61%), asteroids (19%), and penaeid by a bottom thermal front that moves seasonally, shrimp (5%) were the most abundant groups. The located 10 to 20 km from the coast during the austral macrofauna was mostly represented by polychaetes summer and 40-50 km offshore during the winter. (59%), amphipods (14%), and ophiuroids (7%) during During the summer, the water column of the middle the winter; while in the summer, polychaetes, shelf is stratified due to the presence of the cold bivalves, and amphipods made up 54%, 12%, and 10% SACW on the bottom and the CW (near the coast) and of the total abundance, respectively (PIRES-VANIN et TW (offshore) in the upper layer (CASTRO FILHO: al., 2006; PIRES-VANIN et al., 2007). MIRANDA, 1998). In the Santos region, the surface As a whole, in both periods shrimp were an water was warmer and the intrusion of the SACW was important food source in the shallower areas (bay and stronger during the summer 2006, and the mixing of inner shelf) and ophiuroids on the middle shelf. In the SACW with CW occurred near the coast (PIRES- Ubatuba and São Sebastião, located to the north of VANIN et al., 2007). Santos, there is high correlation between fish biomass, The dynamics of the nutrient poor water especially sciaenids, and shrimp biomass (SOUZA et masses (CW and TW) and the nutrient enriched al., 2008). The dietary analysis of 33 fish of Santos SACW play an important role in the distribution of Bay and Perequê beach showed that shrimp, fish (ROSSI-WONGTSCHOWSKI; PAES, 1993; polychaetes, and teleosteans were the main food ROCHA; ROSSI-WONGTSCHOWSKI, 1998; resource ingested. However, although Xiphopenaeus

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kroyeri was consumed by many species, Acetes ACKNOWLEDGMENTS americanus (sergestid) was the major shrimp in the stomach contents (RODRIGUES; MEIRA, 1988), as Financial support for the project ECOSAN found in our study. was provided by the State of São Paulo Research Polychaetes were an abundant food resource Foundation (FAPESP/PRONEX n° 2003/09932-1). in all areas and seasons investigated, thus the greater This study is part of the post-doc project of Elizabeti number of fish species using that resource in the Y. Muto sponsored by FAPESP (Proc. n. 06/56974-0) summer may have resulted from the greater sampling and CNPq (Proc. n. 150 422/2005-9). Scientific effort expended in that season instead of being due to Initiation fellowships were granted to Arantes, L.P.L. the scarcity of this prey during the winter. Crabs were (FAPESP Proc. n. 2007/03252-0), Chalom, A. and mainly consumed during the summer, as well as Coelho, L.I. (PIBIC/CNPq/USP). The authors are copepods. The considerable contribution of crabs for grateful to the crew of the RV Prof. W. Besnard for the fish on the shelf in this period might be related to their support with the fish collection. We wish to the higher abundance of these prey express our thanks to Prof. Dr Edmundo Nonato and items associated with the water mass dynamics. Dr Monica Petti (IO-USP) for their help in identifying During the summer, the most abundant brachyurans on some invertebrates, as well as to the two anonymous the shelf were Portunus spinicarpus, P. spinimanus, reviewers for their valuableon comments on the and Leurocyclus tuberculosus; the former manuscript. predominated on the MS (PIRES-VANIN et al., 2007). The distribution patterns of P. spinicarpus and X. kroyeri on the shelf are linked to the presence of REFERENCES different water masses; the former is associated with the cold front of South Atlantic Central Water and the ÁVILA-DA-SILVA, A. O.; CARNEIRO, M. H.; MENDONÇA, J. T.; SERVO, G. J. 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(Manuscript received 13 June 2012; revised 02 June 2013; accepted 18 June 2013)